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Plant Systematics and Evolution

, Volume 298, Issue 1, pp 155–164 | Cite as

Population genetics and fitness in fragmented populations of the dioecious and endangered Silene otites (Caryophyllaceae)

  • Daniel LauterbachEmail author
  • Michael Ristow
  • Birgit Gemeinholzer
Original Article

Abstract

Population fragmentation is often correlated with loss of genetic diversity and reduced fitness. Obligate out-crossing (dioecy) is expected to enhance genetic diversity, reduce genetic differentiation, and avoid inbreeding depression through frequent gene flow. However, in highly fragmented populations dioecy has only diminishing effects upon genetic structure as pollination limitations (e.g. flight distance of pollinators) most often restrict inter-population gene flow in insect pollinated species. In fragmented dry grasslands in northeastern Germany, we analysed genetic structure, fitness, and habitat quality of the endangered dioecious Silene otites (Caryophyllaceae). Using AFLP markers, a high level of differentiation among ten populations was found (F st = 0.36), while the intra-population genetic diversities (H E = 0.165–0.240) were similar as compared to hermaphroditic species. There was neither a correlation between geographic and genetic distance nor between genetic diversity and population size, which indicates reduced gene flow among populations and random genetic drift. Plant size was positively correlated with genetic diversity. Seed set and number of juveniles were positively related to population size. Higher total coverage resulted in reduced plant fitness, and the number of juveniles was negatively correlated to cryptogam cover. Additionally, we found a sex ratio bias towards more male plants in larger populations. Overall, our results indicate that on a regional geographic scale dioecy does not necessarily prevent genetic erosion in the case of habitat fragmentation, especially in the absence of long distance seed and pollen dispersal capacity.

Keywords

AFLP Population size Mating system Isolation by distance Sex ratio 

Notes

Acknowledgments

This work was funded by the DBU and Heidehofstiftung. We would like to thank the local nature conservation authorities for the collection permission in conservation areas and Hans Pfestorf for help in the field.

References

  1. Barrett SCH (2010) Understanding plant reproductive diversity. Philos Trans R Soc Lond Ser B 365:99–109CrossRefGoogle Scholar
  2. Barrett SCH, Yakimowski SB, Field DL, Pickup M (2010) Ecological genetics of sex ratios in plant populations. Philos Trans R Soc Lond Ser B 365:2549–2557CrossRefGoogle Scholar
  3. Bates D, Maechler M, Dai B (2008) The lme4 Package. Available at: http://lme4.r-forge.r-project.org/ Accessed 10 June 2009
  4. Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273PubMedCrossRefGoogle Scholar
  5. Booy G, Hendriks RJJ, Smulders MJM, Van Groenendael JM, Vosman B (2000) Genetic diversity and the survival of populations. Plant Biol 2:379–391CrossRefGoogle Scholar
  6. Brantjes NBM, Leemans JAAM (1976) Silene otites (Caryophyllaceae) pollinated by nocturnal Lepidoptera and mosquitoes. Acta Bot Neerl 25:281–295Google Scholar
  7. Campbell D, Duchesne P, Bernatchez L (2003) AFLP utility for population assignment studies: analytical investigation and empirical comparison with microsatellites. Mol Ecol 12:1979–1991PubMedCrossRefGoogle Scholar
  8. Cardé RT (2008) Animal migration: seasonal reversals of migrant moths. Curr Biol 18:1007–1009CrossRefGoogle Scholar
  9. Caruso CM, Case AL (2007) Sex ratio variation in gynodioecious Lobelia siphilitica: effects of population size and geographic location. J Evol Biol 20:1396–1405PubMedCrossRefGoogle Scholar
  10. Case AL, Ashman TL (2007) An experimental test of the effects of resources and sex ratio on maternal fitness and phenotypic selection in gynodioecious Fragaria virginiana. Evolution 61:1900–1911PubMedCrossRefGoogle Scholar
  11. Charlesworth D, Charlesworth B (1990) Inbreeding depression with heterozygote advantage and its effect on selection for modifiers changing the outcrossing rate. Evol 44:870–888CrossRefGoogle Scholar
  12. Crawley M (2007) The R Book. John Wiley, ChichesterCrossRefGoogle Scholar
  13. Duffy KJ, Scopece G, Cozzolino S, Fay MF, Smith RJ, Stout JC (2009) Ecology and genetic of the dense-flowered orchid, Neotinea maculata, at the centre and edge of its range. Ann Bot 104:507–516PubMedCrossRefGoogle Scholar
  14. Duminil J, Hardy OJ, Petit RJ (2009) Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure. BMC Evol Biol 9:177PubMedCrossRefGoogle Scholar
  15. Ehrich D (2006) AFLPdat: a collection of R functions for convenient handling of AFLP data. Mol Ecol Notes 6:603–604CrossRefGoogle Scholar
  16. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Sys 24:217–242CrossRefGoogle Scholar
  17. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  18. Excoffier LGL, Schneider S (2006) Arlequin ver. 3.1: an integrated software package for population genetics data analysis. Computational and molecular population genetics lab (CMPG), University of Berne, Swizerland. Accessed 10 June 2008Google Scholar
  19. Fischer M, Matthies D (1998) Effects of population size on performance in the rare plant Gentianella germanica. J Ecol 86:195–204CrossRefGoogle Scholar
  20. Freeman DC, Klikoff LG, Harper KT (1976) Differential resource utilization by the sexes of dioecious plants. Science 193:597–599PubMedCrossRefGoogle Scholar
  21. Giles BE, Goudet J (1997) Genetic differentiation in Silene dioica metapopulations: estimation of spatiotemporal effects in a successional plant species. Am Nat 149:507–526CrossRefGoogle Scholar
  22. Glemin S, Bazin E, Charlesworth D (2006) Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc R Soc B Biol Sci 273:3011–3019CrossRefGoogle Scholar
  23. Guibert C, Civeyrel L, Linder P (2009) Male and female separation event trapped in a species tree. Taxon 58:172–180Google Scholar
  24. Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond Ser B Biol Sci 351:1291–1298CrossRefGoogle Scholar
  25. Hensen I, Oberprieler C (2005) Effects of population size on genetics diversity and seed production in the rare Dictamnus albus (Rutaceae) in Central Germany. Cons Gen 6:63–73CrossRefGoogle Scholar
  26. Hensen I, Oberprieler C, Wesche K (2005) Genetic structure, population size, and seed production of Pulsatilla vulgaris Mill. (Ranunculaceae) in Central Germany. Flora 200:3–14CrossRefGoogle Scholar
  27. Hensen I, Kilian C, Wagner V, Durka W, Pusch J, Wesche K (2010) Low genetic variability and strong differentiation among isolated populations of the rare steppe grass Stipa capillata L. in Central Europe. Plant Biol 12:526–536PubMedCrossRefGoogle Scholar
  28. Hilfiker K, Holderegger R, Rotach P, Gugerli F (2004) Dynamics of genetic variation in Taxus baccata: local versus regional perspectives. Can J Bot 82:219–227CrossRefGoogle Scholar
  29. Honnay O, Jacquemyn H (2007) Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Cons Biol 21:823–831CrossRefGoogle Scholar
  30. Honnay O, Adriaens D, Coart E, Jacquemyn H, Roldan-Ruiz I (2007) Genetic diversity within and between remnant populations of the endangered calcareous grassland plant Globularia bisnagarica L. Cons Genet 8:293–303CrossRefGoogle Scholar
  31. Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evol 50:54–70CrossRefGoogle Scholar
  32. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806PubMedCrossRefGoogle Scholar
  33. Jennersten O, Nilsson SG (1993) Insect flower visitation frequency and seed production in relation to patch size of Viscaria vulgaris (Caryophyllaceae). Oikos 68:283–292CrossRefGoogle Scholar
  34. Jhumur US, Dötterl S, Jürgens A (2008) Floral odors of Silene otites: their variability and attractiveness to mosquitoes. J Chem Ecol 34:14–25PubMedCrossRefGoogle Scholar
  35. Kalliovirta M, Ryttari T, Heikkinen RK (2006) Population structure of a threatened plant, Pulsatilla patens, in boreal forests: modelling relationships to overgrowth and site closure. Biodiv Cons 15:3095–3108CrossRefGoogle Scholar
  36. Korneck D, Schnittler M, Vollmer I (1996) Rote Liste der Farn- und Blütenpflanzen (Pteridophyta et Spermatophyta) Deutschlands. Schriftenreihe für Vegetationskunde 28:21–187Google Scholar
  37. Kwak MM, Velterop O, van Andel J (1998) Pollen and gene flow in fragmented habitats. Appl Veg Sci 1:37–54CrossRefGoogle Scholar
  38. Langhans TM, Storm C, Schwabe A (2009) Biological soil crusts and their microenvironment: Impact on emergence, survival and establishment of seedlings. Flora 204:157–168CrossRefGoogle Scholar
  39. Lauterbach D, Burkart M, Gemeinholzer B (accepted) Rapid genetic differentiation between ex situ and their in situ source populations: an example of the endangered Silene otites (Caryophyllaceae). Bot J Linn SocGoogle Scholar
  40. Lauterbach D, Ristow M, Gemeinholzer B (2011) Genetic population structure, fitness variation and the importance of population history in remnant populations of the endangered plant Silene chlorantha (Willd.) Ehrh. (Caryophyllaceae). Plant Biol 13:667–777PubMedCrossRefGoogle Scholar
  41. Leimu R (2010) Habitat quality and population size as determinants of performance of two endangered hemiparasites. Ann Bot Fennici 47:1–13Google Scholar
  42. Leimu R, Mutikainen P (2005) Population history, mating system, and fitness variation in a perennial herb with a fragmented distribution. Cons Biol 19:349–356CrossRefGoogle Scholar
  43. Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952CrossRefGoogle Scholar
  44. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Ann Rev Ecol Sys 27:237–277CrossRefGoogle Scholar
  45. Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Ann Rev Ecol Sys 15:65–95CrossRefGoogle Scholar
  46. Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99PubMedCrossRefGoogle Scholar
  47. Maurer K, Weyand A, Fischer M, Stöcklin J (2006) Old cultural traditions, in addition to land use and topography, are shaping plant diversity of grasslands in the Alps. Biol Conserv 130:438–446CrossRefGoogle Scholar
  48. Moyle LC (2006) Correlates of genetic differentiation and isolation by distance in 17 congeneric Silene species. Mol Ecol 15:1067–1081PubMedCrossRefGoogle Scholar
  49. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  50. Nilsson E, Agren J (2006) Population size, female fecundity, and sex ratio variation in gynodioecious Plantago maritima. J Evol Biol 19:825–833PubMedCrossRefGoogle Scholar
  51. Obbard DJ, Harris SA, Pannell JR (2006) Sexual systems and population genetic structure in an annual plant: testing the metapopulation model. Am Nat 167:354–366PubMedCrossRefGoogle Scholar
  52. Paschke M, Abs C, Schmid B (2002) Relationship between population size, allozyme variation, and plant performance in a narrow endemic Cochlearia bavarcia. Cons Gen 3:131–144CrossRefGoogle Scholar
  53. Peterson A, Bartish IV, Peterson J (2008) Effects of population size on genetic diversity, fitness and pollinator community composition in fragmented populations of Anthericum liliago L. Plant Ecol 198:101–110CrossRefGoogle Scholar
  54. Pless H (1994) Pflanzensoziologische Untersuchungen der Trockenrasen an den Hängen des Odertales im Kreis Seelow (Brandenburg). Diplomarbeit, GöttingenGoogle Scholar
  55. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes consequences, and solutions. Nat Rev Genet 6:847–859PubMedCrossRefGoogle Scholar
  56. Poschlod P, WallisDeVries MF (2002) The historical and socioeconomic perspective of calcareous grasslands–lessons from the distant and recent past. Biol Cons 104:361–376CrossRefGoogle Scholar
  57. Poschlod P, Bakker JP, Kahmen S (2005) Changing land use and its impact on biodiversity. Basic Appl Ecol 6:93–98CrossRefGoogle Scholar
  58. Prasse R, Ristow M, Klemm G, Machatzi B, Raus T, Scholz H, Stohr G, Sukopp H, Zimmermann F (2001) Liste der wildwachsenden Gefäßpflanzen des Landes Berlin—mit Roter Liste. Kulturbuch-Verlag, BerlinGoogle Scholar
  59. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  60. Rambaut A (2008) FigTree v1.2. Available at http://tree.bio.ed.ac.uk/software/FigTree/. Accessed 10 June 2009
  61. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org. Accessed June 2008
  62. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Cons Biol 17:230–237CrossRefGoogle Scholar
  63. Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606CrossRefGoogle Scholar
  64. Richards CN, Emery SN, McCauley DE (2003) Genetic and demographic dynamics of small populations of Silene latifolia. Heredity 90:181–186PubMedCrossRefGoogle Scholar
  65. Ristow M, Herrmann A, Illig H, Klemm G, Kummer V, Kläge HC, Machatzi B, Rätzel S, Schwarz R, Zimmermann F (2006) Liste und Rote Liste der etablierten Gefäßpflanzen Brandenburgs. Naturschutz und Landschaftspflege in Brandenburg 15(4):1–163Google Scholar
  66. Ronikier M (2002) The use of AFLP markers in conservation genetics—a case study on Pulsatilla vernalis in the polish lowlands. Cell Mol Biol Lett 7:677–684PubMedGoogle Scholar
  67. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  68. Schmidt K, Jensen K (2000) Genetic structure and AFLP variation of remnant populations in the rare plant Pedicularis palustris (Scrophulariaceae) and its relation to population size and reproductive components. Am J Bot 87:678–689PubMedCrossRefGoogle Scholar
  69. Schulz A (1905) Das Blühen von Silene otites. Beihefte zum Botanischen Zentralblatt 18:433–446Google Scholar
  70. Singh M, Chabane K, Valkoun J, Blake T (2006) Optimum sample size for estimating gene diversity in wild wheat using AFLP markers. Genet Resour Crop Evol 53:23–33CrossRefGoogle Scholar
  71. Soldaat LL, Vetter B, Klotz S (1997) Sex ratio in populations of Silene otites in relation to vegetation cover, population size and fungal infection. J Veget Sci 8:697–702CrossRefGoogle Scholar
  72. Soldaat LL, Lorenz H, Trefflich A (2000) The effect of drought stress on the sex ratio variation of Silene otites. Folia Geobotanica 35:203–210CrossRefGoogle Scholar
  73. Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440CrossRefGoogle Scholar
  74. Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  75. Tero N, Aspi J, Siikamäki P, Jäkäläniemi A, Tuomi J (2003) Genetic structure and gene flow in a metapopulation of an endangered plant species, Silene tatarica. Mol Ecol 12:2073–2085PubMedCrossRefGoogle Scholar
  76. Tsuda Y, Komagata O, Kasai S, Hayashi T, Nihei N, Saito K, Mizutani M, Kunida M, Yoshida M, Kobayashi M (2008) A mark-release-recapture study on dispersal and flight distance of Culex pipiens pallens in an urban area of Japan. J Am Mosq Control Assoc 24:339–343PubMedCrossRefGoogle Scholar
  77. Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (1993) Flora Europaea Vol. 1. Psilotaceae to Platanaceae, second ed. Cambridge University Press, CambridgeGoogle Scholar
  78. Ueno N, Suyama Y, Seiwa K (2007) What makes the sex ratio female-biased in the dioecious tree Salix sachalinensis? J Ecol 95:951–959CrossRefGoogle Scholar
  79. Vandepitte K, Honnay O, De Meyer T, Jacquemyn H, Roldan-Ruiz I (2010) Patterns of sex ratio variation and genetic diversity in the dioecious forest perennial Mercurialis perennis. Plant Ecol 206:105–114CrossRefGoogle Scholar
  80. Vekemans X (2002) AFLP-SURV version 1.0. Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, BelgiumGoogle Scholar
  81. Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Springer, New YorkGoogle Scholar
  82. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  83. Watt AS (1981) A comparison of grazed and ungrazed grassland a in East Anglian breckland. J Ecol 69:499–508CrossRefGoogle Scholar
  84. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol 38:1358–1370CrossRefGoogle Scholar
  85. Wessels-de Wit S, Schwabe A (2010) The fate of sheep-dispersed seeds: Plant species emergence and spatial patterns. Flora 205:56–665Google Scholar
  86. Wilson WG, Harder LD (2003) Reproductive uncertainty and the relative competiveness of simultaneous hermaphroditism versus dioecy. Am Nat 162:220–241PubMedCrossRefGoogle Scholar
  87. Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. TREE 11:413–418PubMedGoogle Scholar
  88. Zhivotovsky LA (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Mol Ecol 8:907–913PubMedCrossRefGoogle Scholar
  89. Zhou HP, Chen J (2010) Spatial genetic structure in an understorey dioecious fig species: the roles of seed rain, seed and pollen-mediated gene flow, and local selection. J Ecol 98:1168–1177CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Daniel Lauterbach
    • 1
    • 2
    Email author
  • Michael Ristow
    • 3
  • Birgit Gemeinholzer
    • 4
  1. 1.Botanic Garden and Botanical Museum Berlin-DahlemFreie Universität BerlinBerlinGermany
  2. 2.Institute of EcologyTechnische Universität BerlinBerlinGermany
  3. 3.Plant Ecology and Nature Conservation, Institute for Biochemistry and BiologyUniversity of PotsdamPotsdamGermany
  4. 4.AG Spezielle BotanikJustus-Liebig-Universität GiessenGiessenGermany

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